Temporally stable adaptation is robust, incomplete and specific

Sensorimotor adaptation, the process that reduces movement errors by learning from sensory feedback, is often studied within a session of about half an hour. Within such a single session, adaptation generally reaches plateau before errors are completely removed. However, adaptation may complete on longer timescales: the slow components of error‐based adaptation are associated with good retention. In this study, we tested how adaptation evolves over time by asking participants to perform six adaptation sessions on different days. In these sessions, participants performed a three‐dimensional reaching task while visual feedback about endpoint errors was rotated around the cyclopean eye. In addition, context specificity of the adaptation was addressed by measuring inter‐limb transfer and transfer to visual and proprioceptive perceptual tasks. We show that from the second session on, the adaptation was retained almost completely across sessions. However, after six learning sessions, adaptation still reached plateau before errors were completely removed. The adaptation was specific: the adaptation did neither transfer to the other hand, nor to the visual, and only marginally to the proprioceptive perceptual estimates. We conclude that motor adaptation is robust, specific and incomplete.

[1]  M M Cohen,et al.  Continuous versus Terminal Visual Feedback in Prism Aftereffects , 1967, Perceptual and motor skills.

[2]  C. Prablanc,et al.  Partitioning the components of visuomotor adaptation to prism-altered distance , 2011, Neuropsychologia.

[3]  Mathias Hegele,et al.  Generalization of implicit and explicit adjustments to visuomotor rotations across the workspace in younger and older adults. , 2011, Journal of neurophysiology.

[4]  J. Rothwell,et al.  The dissociable effects of punishment and reward on motor learning , 2015, Nature Neuroscience.

[5]  Yves Rossetti,et al.  Enhancing Visuomotor Adaptation by Reducing Error Signals: Single-step (Aware) versus Multiple-step (Unaware) Exposure to Wedge Prisms , 2007, Journal of Cognitive Neuroscience.

[6]  Philip N. Sabes,et al.  Calibration of visually guided reaching is driven by error-corrective learning and internal dynamics. , 2007, Journal of neurophysiology.

[7]  S. Wise,et al.  Mechanisms of use-dependent plasticity in the human motor cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[8]  B Wallace,et al.  Components of prism adaptation in terminal and concurrent exposure: Organization of the eye-hand coordination loop , 1988, Perception & psychophysics.

[9]  Juan Fernández-Ruiz,et al.  Decay of prism aftereffects under passive and active conditions. , 2004, Brain research. Cognitive brain research.

[10]  David M. Huberdeau,et al.  Dual-process decomposition in human sensorimotor adaptation , 2015, Current Opinion in Neurobiology.

[11]  D. Henriques,et al.  Sensory recalibration of hand position following visuomotor adaptation. , 2009, Journal of neurophysiology.

[12]  D. Wolpert,et al.  Context-Dependent Decay of Motor Memories during Skill Acquisition , 2013, Current Biology.

[14]  David M. Huberdeau,et al.  The Influence of Movement Preparation Time on the Expression of Visuomotor Learning and Savings , 2015, The Journal of Neuroscience.

[15]  K. van der Kooij,et al.  Rewarding imperfect motor performance reduces adaptive changes , 2016, Experimental Brain Research.

[16]  Konrad Paul Kording,et al.  Relevance of error: what drives motor adaptation? , 2009, Journal of neurophysiology.

[17]  L. K. Canon,et al.  Influence of concurrent and terminal exposure conditions on the nature of perceptual adaptation. , 1971, Journal of experimental psychology.

[18]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[19]  M. Ernst,et al.  The statistical determinants of adaptation rate in human reaching. , 2008, Journal of vision.

[20]  D. Henriques,et al.  Proprioceptive recalibration arises slowly compared to reach adaptation , 2016, Experimental Brain Research.

[21]  Raymond J. Delnicki,et al.  Overcoming Motor “Forgetting” Through Reinforcement Of Learned Actions , 2012, The Journal of Neuroscience.

[22]  Felice L. Bedford,et al.  Perceptual and cognitive spatial learning. , 1993, Journal of experimental psychology. Human perception and performance.

[23]  M. Hinder,et al.  The contribution of visual feedback to visuomotor adaptation: How much and when? , 2008, Brain Research.

[24]  Daniel M Wolpert,et al.  Adaptation to a visuomotor shift depends on the starting posture. , 2002, Journal of neurophysiology.

[25]  R. Shadmehr,et al.  Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning , 2006, PLoS biology.

[26]  Wilsaan M. Joiner,et al.  Long-term retention explained by a model of short-term learning in the adaptive control of reaching. , 2008, Journal of neurophysiology.

[27]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  J.B.J. Smeets,et al.  A new binocular cue for absolute distance: Disparity relative to the most distant structure , 2010, Vision Research.

[29]  Eli Brenner,et al.  Visuomotor Adaptation: How Forgetting Keeps Us Conservative , 2015, PloS one.

[30]  J. Krakauer,et al.  An Implicit Plan Overrides an Explicit Strategy during Visuomotor Adaptation , 2006, The Journal of Neuroscience.

[31]  J B J Smeets,et al.  Alignment to natural and imposed mismatches between the senses. , 2013, Journal of neurophysiology.

[32]  Ian P. Howard,et al.  Additivity of components of prismatic adaptation , 1974 .

[33]  Reza Shadmehr,et al.  A memory of errors in sensorimotor learning , 2014, Science.

[34]  Claude Ghez,et al.  Separate adaptive mechanisms for controlling trajectory and final position in reaching. , 2007, Journal of neurophysiology.

[35]  Robert L. Sainburg,et al.  Mechanisms underlying interlimb transfer of visuomotor rotations , 2003, Experimental Brain Research.

[36]  Vincent S. Huang,et al.  Rethinking Motor Learning and Savings in Adaptation Paradigms: Model-Free Memory for Successful Actions Combines with Internal Models , 2011, Neuron.

[37]  R B Welch,et al.  Variables affecting the intermanual transfer and decay of prism adaptation. , 1974, Journal of experimental psychology.